One of the most important discoveries yet made about the nervous system was that nerve fibers work by electricity. This was Galvani’s finding, part of Mary Shelley’s inspiration in writing Frankenstein (Tropp, 1976). Nearly as momentous was the finding that chemicals carry messages from neuron to neuron. This was discovered when Otto Loewi was conducting experiments of electrically stimulating the vagus nerve of a frog; this stimulation slowed down its heart (Brazier, 1959). If during stimulation Loewi bathed the frog’s heart in fluid and then applied this fluid to the heart of a second frog, then this second frog’s heart slowed down, too. He inferred that some chemical substance was released into the fluid by the nerve endings of the first frog and was then responsible for slowing down the heart of the second. The substance was acetylcholine. Subsequently more than 50 substances have been discovered that are released by regions in the nervous system and have effects on other neurons, or on glands or muscles.
Neurochemicals can be thought of in three functional families that overlap with each other. The first family is neurotransmitters, which are released into the synapses of neurons. As well as acetylcholine they include norepinephrine, dopamine, serotonin, and gamma-amino butyric acid. Transmitter substances are released by nerve impulses from the end of a neuron’s axon. They diffuse in milliseconds across the tiny synaptic gaps between cells to activate or inhibit the receiving neuron or muscle fiber.
Second, there are hormones: substances carried in the blood to affect organs that are sensitive to them. In their usual functions, hormones take longer to act than transmitter substances and their effects last longer. The substances include both small molecules like adrenaline and cortisol
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FIGURE 6.3 Mean scores at age 38 months on an index indicating relatively more EEG activation on the left as compared to the right hemisphere of children who at age 31 months had been classified as inhibited, middle, or uninhibited in a 25-minute play session (Davidson, 1992a).
(see Chapter 5), and also peptides. The principal gland that controls most hormonal systems is the pituitary, which is joined to, and largely controlled by, the hypothalamus. Other glands remote from the brain such as the adrenal glands also release hormones that have effects on the body and in some cases also on neurons in the hypothalamus.
Third, there is a group of substances that are neuro-modulators. Many of them are peptides. Endogenous opiates (chemically similar to drugs like opium and heroin), for example, modulate the pain system, and other peptides (such as cholecystokinin) have important emotional effects. Some peptides are transmitters, but when they act as neuro-modulators they are released by some neurons, and diffuse some distance to affect many thousands of nearby neurons.
The study of different neurochemicals has helped us think how emotions are represented in the nervous system: neurochemicals are located anatomically in networks in regions of the brain and related to functionally distinct classes of behavior (e.g., Panksepp, 1986; 1998). Neurochemicals can also be administered to individuals in different ways, allowing research- ers to study how they influence emotions, moods, and other psychological states. Here we’ll review ideas about two of the most widely studied neurochemicals and their relevance to emotion: serotonin and oxytocin.
Serotonin
Serotonin is a neurotransmitter produced widely throughout the brain, in particular targeting subcortical areas (amygdala, ventral striatum, hypothalamus) as well as regions of the prefrontal cortex. It has come to be of interest because of the widespread use of serotonin-reuptake inhibitors like Prozac (chemical name, fluoxetine) as antidepressants, which are calculated to increase availability of brain serotonin. It is estimated that nearly 10% of Americans take antidepressants. As we shall see, however, in Chapter 13, it is likely that the efficacy of these substances in alleviating depression has been overestimated.
The question for this chapter is how serotonin may influence emotions and moods. In a synthetic review of the literature on serotonin, Charles Carver and his colleagues (2008) propose that brain mechanisms that use serotonin are involved in the balance between fast, emotional, associationistic processing in the subcortex and slower, deliberate, language-based processing in the frontal lobes. In cognitive terms, these have become known respectively as heuristic and deliberative processes—fast and slow thinking as Kahneman (2011) has called them—and we discuss them further in Chapter 10. When serotonin levels in the synapses of your brain are low, Carver et al. say your fast, intuitive subcortical reactions in regions like the amygdala or nucleus accumbens tend to predominate over the more deliberative, prefrontally based processes.
This framework may help to explain paradoxical findings related to serotonin. For example, low levels of serotonin are associated with two kinds of emotional disorders. The first is antisocial tendencies, in which the individual is prone to impulsive and aggressive outbursts. The second is depression, where the individual feels high levels of negative emotion. On the surface one might find contradiction in the idea that low levels of serotonin are associated with both antisocial and depressive tendencies. But in the treatment of Carver and colleagues, both antisocial behavior and depression reflect an imbalance in the influence of frontal lobes upon subcortical processes: in the case of antisocial people, the frontal lobes are not regulating aggressive tendencies; in depressives, the frontal lobes are not regulating negative emotions.
According to this idea, serotonin levels produce an imbalance in the interaction between subcortical and cortical regions of the brain that can lead to problematic aggression (if the person is prone to antisocial impulsivity) or depression (if the person is prone to negative affect and distress).
With respect to personality, Carver and colleagues summarize studies that fit with the notion that serotonin modulates the interaction between subcortical and cortical processes. Low levels of serotonin tend to correlate with certain personality traits that reflect diminished activation in prefrontal regions of the brain involved in emotion regulation: low levels of Agreeableness (that is to say hostility), high levels of Neuroticism (defined by increased emotional reactivity), and low levels of constraint (which reflect the individual’s ability to be future oriented and able to modify impulses according to the current social context). Carver et al. argue that when serotonin levels are low, subcortical regions override the prefrontal regulation of impulses.
Carver et al. cite, for instance, experiments such as those of Brian Knutson and his colleagues (1998) in which a serotonin reuptake inhibitor (assumed to increase the brain’s available serotonin) was given to some volunteers and a placebo was administered to others. Compared to participants in the placebo condition, those given the serotonin reuptake inhibitor were found to have decreased indices of hostility and negative affect as measured by personality tests, and showed more cooperation and affiliation as they played a puzzle game together. Carver et al. also cite subsequent studies in which, with experimental increases in serotonin, people were found to be less reactive to stressful events.
Oxytocin
Oxytocin is a peptide of nine amino acids. It is produced in the hypothalamus and released into both brain and bloodstream. Receptors for this peptide are found in the olfactory system, limbic-hypothalamic system, the periaqueductal gray, and regions of the spinal cord that regulate the autonomic nervous system, especially the parasympathetic branch (Uvnas- Moberg, 1994). Oxytocin is involved in lactation, maternal bonding, and sexual interaction (Carter, 1992). In the most general sense, oxytocin promotes bonding behavior possibly by reducing anxiety (Carter & Altemus, 1997; Taylor et al., 2000) and making social contact and affiliation pleasant (Insel, Young, & Zuoxin, 1997; Panksepp, 1998). Given these basic facts about oxytocin, early theorizing posited that oxytocin might be thought to be one biological substrate of love (Carter, 1998; Insel, 1993).
First, comparisons between prairie voles who display pair-bonding, and the closely related montane voles, who do not pair-bond, have revealed differences in the location of oxytocin receptors in the brains of each species (Carter, 1998; Insel et al., 1997). Moreover, in the prairie vole injections of oxytocin directly into specific areas of the brain have been found to increase preferences for a single partner over other partners, whereas injections of oxytocin antagonists depress single-partner preference (Williams, Insel, Harbaugh, & Carter, 1994). Other studies of voles find that mating stimulates oxytocin release (Carter, 1992), and blocking the activity of oxytocin prevents maternal behavior (Insel & Harbaugh, 1989; Pederson, 1997). Prosocial behavior was found to increase and aggression to decrease when female prairie voles were given oxytocin (Witt et al., 1990). Male and female prairie voles increase their social contact after oxytocin treatment (Witt et al., 1992).
Studies of other species likewise reveal similar social bonding functions of oxytocin. In primates, injections of oxytocin have led to increases in the frequency of touching and watching infants, and decreases in aggressive yawns and facial threats (Holman & Goy, 1995). Separation distress calls in isolated domestic chicks have been found to decrease after oxytocin treatment (Panksepp et al., 1997). Oxytocin injections have caused ewes to become attached to unfamiliar lambs (Keverne et al., 1997). Rat pups show preferences for odors of mothers, except when pretreated with oxytocin antagonists (Nelson & Panksepp, 1996).
In humans, early studies found suggestive evidence in support of the thesis that oxytocin promotes bonding. In studies of lactating women, it has been found that oxytocin reduces activity of the hypothalamic-pituitary axis (Carter & Altemus, 1997; Uvnas-Moberg, 1997, 1998). Massage leads to increased oxytocin release in the bloodstream (Turner et al., 1999, 2002). Oxytocin has been found to be released during sexual activity (Carmichael et al., 1987; Murphy, Seckl, Burton, Checkley, & Lightman, 1987). And when women were asked to recount an experience of warmth felt toward another person, their nonverbal display of love—evident in smiling, head tilts, and open- handed gestures—correlated with an increase in oxytocin released into the bloodstream (Gonzaga et al., 2006). And what’s true of individuals is true of couples. Dietzen and colleagues have found that heterosexual couples who inhaled oxytocin through a nasal spray prior to discussing an issue of conflict, compared to couples in a control condition in which partners inhaled a neutral solution, showed more positive relational behaviors—validation, caring, eye contact, smiling—and they had lower levels of the stress hormone after the conflict (Dietzen et al., 2009).
These early findings relating oxytocin to bonding and love have led investigators to the thesis that oxytocin may promote prosocial behavior toward others more generally. Dozens of studies have focused on two more specific hypotheses. A first is that oxytocin promotes generosity. For example, in one seminal study in this literature, participants played the trust game with another player (Kosfeld et al., 2005). In the trust game, one participant, known as the “investor,” makes contributions to another individual, known as the “trustee.” The value of the money given to the trustee then triples, and the trustee then gives some amount back to the investor—as much or as little as he or she desires. In this particular study, participants either whiffed some oxytocin in a nasal spray, or a neutral control solution. As you can see in Figure 6.4, participants given oxytocin were
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FIGURE 6.4 Participants given oxytocin are more likely to share the maximum amount of money in an economic game (adapted from Kosfeld et al., 2005).
more than twice as likely as those in the control condition to give away the maximum amount of money to a stranger.
A second interest is whether oxytocin increases our empathic responses to others. For example, in one study on this point, Domes and colleagues (Domes et al., 2007) had participants inhale oxytocin or a control solution in a nasal spray. They then were given 36 pictures in which people expressed different emotions in subtle expressions of the eyes—a task known as the Mind-in-the-Eyes task. Those participants who were given oxytocin performed better on this task, proving to be better able to read emotion in subtle expressions in the eyes, in particular more difficult expressions.
These studies relating oxytocin to increased love, positive communication, prosocial behavior, and empathy in humans generated a great deal of excitement—oxytocin was heralded as the love drug, as a potential cure for certain disorders defined by difficulties in social connection, such as autism, and a means by which to build trust and social ties in communities (there is even an oxytocin spray available in England!). More recent reviews and scientific studies raise some problems with this view. First of all, a recent review by Jennifer Bartz and her colleagues finds that whereas the influences of oxytocin upon increased prosocial behavior and empathy are often observed in studies, at other times they are not, suggesting that oxytocin does not promote a blind prosociality or empathy toward all (Bartz et al., 2011). Instead, the influences of oxytocin upon prosocial behavior and empathy depend on the specifics of the social context—for example, whether you are interacting with friend or foe—and the individual’s personality. In their review, Bartz and colleagues suggest that oxytocin instead promotes a greater social sensitivity to salient social cues within the context. Recent work by Carsten de Dreu and his colleagues (2010) also points to a more nuanced view of oxytocin, suggesting that oxytocin promotes a particular kind of prosociality—that directed toward the in-group, but not toward the out-group. A series of ingenious studies by de Dreu and his colleagues has found that oxytocin most potently promotes in-group favoritism, the preferential evaluation and treatment of one’s own group relative to out-groups. In one series of studies, inhaling oxytocin compared to a control solution led participants to allocate more resources to their own group rather than to themselves (the preferred choice of control participants), to trust their in-group more, and, in conditions of high fear, to avoid cooperation with an out-group. In another investigation, participants who inhaled oxytocin relative to the control participants showed evidence of more automatic positive evaluations of their own group, they were more likely to assume their own group experienced complex moral emotions like embarrassment, and they were less likely to be willing to sacrifice a member of their own group to save the lives of several individuals in a moral decision-making task (de Dreu et al., 2011). It would appear that oxytocin promotes a more parochial form of altruism and empathy, one that benefits one’s own group over others.
S U M M A R Y
In this chapter we turned toward the human brain to explore what regions might be involved in emotion, and in what ways. We reviewed current understandings of how the brain works and how different regions of the brain serve different func- tions. We considered different methods for the study of the brain, ranging from studies of patients with brain damage to the imaging of brain regional activity as humans respond to
different stimuli, and the effects of psychoactive drugs. We then focused our attention on subcortical processes involved in emotion. In this section, we saw that a small portion of the forebrain, the amygdala, is involved in assigning, at an unconscious level, emotional significance to events, that the nucleus accumbens signals the potential rewards of different stimuli, and that the periaqueductal gray in the
midbrain is related to the reduction of the experience of pain, and caregiving. We then looked at cortical processes related to emotion, focusing on regions of the cortex involved in empathy, emotion regulation, social pain, and positive emo- tion. Finally, we turned our attention to the role of two neurochemicals involved in emotion. Serotonin may be
involved in balancing subcortical and cortical processes involved in emotion. Oxytocin has been thought of as a biological underpinning of love and devotion, although more recent studies suggest oxytocin may be more aptly thought of as a neurochemical that promotes social sensitivity.
T O T H I N K A B O U T A N D D I S C U S S 1. What would be definitive evidence for you to sort out
whether the amygdala is activated by fear, valence, or the intensity of a stimulus?
2. What are some specific emotions that map onto wanting versus liking, or anticipating pleasure versus consuming pleasurable things?
3. Design a study that would clarify whether oxytocin is fundamentally related to social affection versus more general social sensitivity.
F U R T H E R R E A D I N G
An excellent and wide-ranging introduction to affective neuroscience:
Panksepp, J., & Biven, L. (2012). The archaelogy of mind: Neuroevolutionary origins of human emotions. New York, NY. WW Norton.
For an outstanding recent review of affective neuroscience, read:
K. N. Ochsner (2008). The social-emotional processing stream: Five core constructs and their translational
potential for schizophrenia and beyond. Biological Psy- chiatry, 64, 48–61.
For the most recent summary of LeDoux’s influential work, see:
S. M. Rodrigues, J. E. LeDoux, & R. M. Sapolsky (2009). The influence of stress hormones on fear circuitry. Annual Review of Neuroscience, 32, 289–313.